Original Article
Effect on Ovarian Reserve of Hemostasis by Bipolar Coagulation Versus Suture During Laparoendoscopic Single-Site Cystectomy for Ovarian Endometriomas Taejong Song, MD, PhD*, Woo Young Kim, MD, Kyo Won Lee, MD, PhD, and Kye Hyun Kim, MD, PhD From the Department of Obstetrics & Gynecology, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea (Drs. Song, W. Y. Kim, Lee, and K. H. Kim), and Department of Obstetrics & Gynecology, CHA Gangnam Medical Center, CHA University, Seoul, Republic of Korea (Dr. Song).
ABSTRACT Study Objective: To compare the postoperative decrease in ovarian reserve between hemostasis by bipolar coagulation and suture during laparoendoscopic single-site cystectomy (LESS-C) for ovarian endometriomas. Design: Prospective comparative study (Canadian Task Force Classification II-1). Setting: University hospital. Patients: One hundred twenty-five patients with ovarian endometriomas. Interventions: Patients with endometrioma were managed by hemostasis with either bipolar coagulation (n 5 62) or suturing (n 5 63) during LESS-C. We evaluated the impact of surgery on ovarian reserve using serum anti-M€ ullerian hormone (AMH) levels, which were measured before surgery and 3 months after surgery in all patients. Measurement and Main Results: Baseline characteristics such as age, bilaterality of endometriomas, and preoperative AMH levels were similar between the 2 study groups. There were also no differences between the 2 groups in surgical outcomes, such as operative time, operative blood loss, or operative complications. In both study groups, postoperative AMH levels were lower than preoperative AMH levels (p , .001). The decline rate of AMH levels was significantly greater in the bipolar coagulation group than in the suture group (42.2% [interquartile range, 16.5%–53.0%] and 24.6% [interquartile range, 11.6%– 37.0%], respectively, p 5 .001). Conclusion: Hemostasis by bipolar coagulation after stripping of the endometrioma during LESS-C reduces ovarian reserve more than suturing does, as determined by serial AMH levels. Therefore, suturing may be a better hemostatic choice after stripping ovarian endometriomas. Journal of Minimally Invasive Gynecology (2015) 22, 415–420 Ó 2015 AAGL. All rights reserved. Keywords:
AMH; Bipolar coagulation; Ovarian cystectomy; Ovarian reserve; Suture
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Laparoscopic cystectomy is a well-established method of management for ovarian endometriomas [1–6]. The surgical procedure is usually performed by stripping the Corresponding author: Taejong Song, MD, PhD, Department of Obstetrics & Gynecology, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, 108 Pyung-dong, Jongno-gu, Seoul 110-746, Republic of Korea. E-mail: [email protected] Submitted September 3, 2014. Accepted for publication November 6, 2014. Available at www.sciencedirect.com and www.jmig.org 1553-4650/$ - see front matter Ó 2015 AAGL. All rights reserved. http://dx.doi.org/10.1016/j.jmig.2014.11.002
endometriotic cyst wall, followed by bleeding control of the ovarian wound ground using bipolar coagulation or suturing. However, the ovarian hemostasis achieved by these 2 methods could result in damage to the ovarian reserve [7–11]. Bipolar coagulation can result in thermal destruction of the surrounding healthy ovarian follicle, whereas a hemostatic suture may result in mechanical damage to normal ovarian tissue and an increase in intraovarian pressure in ischemic regions. Studies that have compared hemostasis by bipolar coagulation versus suturing during laparoscopic ovarian
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cystectomy have not shown consistent effects on ovarian reserve [1,7,12]. Furthermore, no study that has compared these 2 hemostatic methods has been performed in the setting of laparoendoscopic single-site ovarian cystectomy (LESS-C). Because of the increasing patient demand for LESS-C, it is important to determine which hemostatic methods better preserve postoperative ovarian reserve. Therefore, we compared the effects of bipolar coagulation versus suturing on ovarian reserve in patients who underwent LESS-C for ovarian endometriomas. Materials and Methods This was a prospective nonrandomized study of 125 patients who underwent LESS-C for endometriomas between October 2011 and May 2014 at the CHA Gangnam Medical Center, Seoul, Republic of Korea. The 62 patients who underwent LESS-C with hemostasis by bipolar coagulation were compared with 63 patients who underwent LESS-C with hemostasis by suturing to control bleeding from the ovarian wound ground. Group allocation was carried out according to an odd or even procedure, with the first patient being allocated to the suture group, the second to the bipolar coagulation group, and so on. Patients between 18 and 39 years of age, with a maximum diameter of the endometriotic cyst between 3 and 12 cm, regular menstrual bleeding (defined as cycle length between 21 and 45 days), and appropriate medical status for laparoscopic surgery (American Society of Anesthesiologists Physical Status classification 1 or 2) were included in this study. Patients with any suspicious findings of malignant gynecologic disease, postmenopausal status, pregnancy, lactation, any other endocrine disease (such as uncontrolled thyroid dysfunction, hyperprolactinemia, or Cushing syndrome), or use of hormonal treatments in the 3 months before surgery were excluded. After obtaining institutional review board approval for this study, all patients gave written consent for their data to be collected prospectively. All procedures were performed by 1 surgeon (T. Song), who previously managed .200 LESS-C procedures. All patients underwent the same standard preparation before surgery, including the administration of prophylactic antibiotics 30 min before the procedure. The LESS-C technique used was previously described in detail [9]. In brief, after the introduction of general anesthesia, a single multichannel port was inserted through the umbilicus, and a laparoscope was introduced through 1 of the channels. Before initiating the stripping of the endometriotic cyst, the ovary was completely freed by obtuse and sharp dissection. After identifying a cleavage plane between the cyst wall and the ovarian cortex, the ovary was pulled slowly and gently in opposite directions with 2 atraumatic grasping forceps. Once the whole cystic wall was separated from the ovarian cortex, bipolar coagulation or ovarian suturing was applied for hemostasis. In the bipolar coagulation group, complete hemostasis was achieved with a 20- to 30-W current applied using bipolar forceps (Karl Storz, Tuttlingen, Germany) on sites of bleeding in the internal face of the ovary without coagulation of external surface. Bleeding sites were then re-examined by irrigation. In the suture group, hemostasis of the ovarian parenchyma was achieved using a 12-in, 2-0 unidirectional-barbed suture with a 26-mm half circle taper-point needle (V-Loc 90 Absorbable Wound Closure device; Covidien, Mansfield, Massachusetts). The first stitch was locked
Journal of Minimally Invasive Gynecology, Vol 22, No 3, March/April 2015
by a loop at 1 end of the ovarian wound, and then a continuous suture was passed through to the opposite end of the ovarian wound and cut without tying a knot. The ovary was sutured edge-to-edge. No chemical hemostats, except for bipolar coagulation or ovarian suture were allowed in either group. In the bipolar group, no bipolar coagulation was performed during or after stripping of the cysts. The ovarian cysts, which were placed into the specimen retrieval endopouch, were removed through the umbilical single-port. After bleeding was controlled, the single multichannel port was removed, the transumbilical fascia and subcutaneous tissue were approximated and closed layer by layer with 1-0 Vicryl (Ethicon, Somerville, New Jersey), and the skin was closed subcuticularly with 3-0 Vicryl. The primary aim of this study was to compare the effects of 2 hemostatic techniques (bipolar coagulation vs suturing) on ovarian reserve in patients who underwent LESS-C for ovarian endometriomas. The ovarian reserve was assessed by measuring serum AMH levels, which were measured before surgery and 3 months after surgery in all patients. The rate of decline of serum AMH levels was defined as follows: rate of decline (%) 5 100 ! (preoperative AMH level – postoperative AMH level)/preoperative AMH level. The serum was separated from whole blood, transferred to polypropylene tubes, and stored at –70 C until the assay. Serum AMH concentrations were determined using a commercially available enzyme-linked immunosorbent assay kit (Beckman Coulter, Marseille, France). The detection limit of the assay was 0.14 ng/mL, and the intra- and inter-assay coefficients of variation for the AMH assay were .12.3% and .14.2%, respectively. All statistical analyses were performed using SPSS 13.0 (SPSS Inc., Chicago, Illinois). Data are presented as means 6 SD or medians (interquartile range [IQR]) for continuous variables, and frequencies (percentages) for categorical variables. Baseline parameters and study outcomes were compared between the 2 groups using the Student’s t-test or the Mann-Whitney test for continuous variables, and the c2 test or Fisher’s exact test for categorical variables, as appropriate. The serum AMH levels before and after surgery were compared in the same group using the Wilcoxon signed-rank test. Multivariate analysis to determine independent parameters for postoperative ovarian reserve was performed using multiple linear regression. p Values ,.05 were considered statistically significant.
Results Baseline characteristics including age, body mass index, parity, marital status, and abdominal surgical history were similar between the 2 study groups (Table 1). The diameter and location of ovarian cysts and the level of preoperative tumor markers (e.g., cancer antigen-125 and cancer antigen 19-9) also did not differ between the 2 groups. The surgical outcomes of each group are shown in Table 2. The histologic type of ovarian cyst, ovarian surgery performed, operative time (defined as the time from skin incision to skin closure), operative blood loss (calculated as the difference between suction and irrigation), change in hemoglobin (defined as the difference between preoperative hemoglobin level and that at postoperative day 1), and length of hospital stay (defined as the time from the operation day to the day of discharge) were all similar between
Song et al.
Bipolar Coagulation vs Suture in Preserving Ovarian Reserve
417
Table 1 Baseline characteristics Characteristics
Bipolar coagulation group (n 5 62)
Suture group (n 5 63)
Age, yrs Body mass index, kg/m2 Marital status Married or cohabitating Single/separated/widowed/Divorced Parity Nulliparous Parous Menopause Comorbiditiesa Abdominal surgical historyb Preoperative hemoglobin (mg/dL) Diameter of ovarian cyst, cmc Location of ovarian cyst Unilateral Bilateral CA125, IU/mL (IQR) CA19-9, IU/mL (IQR)
31.2 6 4.8 20.6 6 2.6
30.8 6 5.2 20.4 6 2.6
38 (61.3%) 24 (38.7%)
35 (55.6%) 28 (44.4%)
46 (74.2%) 16 (25.8%) 0 4 (6.5%) 12 (19.4%) 12.7 6 0.9 6.4 6 1.6
51 (82.3%) 11 (17.7%) 0 6 (9.5%) 8 (12.9%) 12.9 6 1.0 6.8 6 2.2
46 (74.2%) 16 (25.8%) 25.8 (15.0–48.8) 20.6 (9.4–36.2)
48 (76.2%) 15 (23.8%) 22.2 (14.0–42.9) 17.1 (11.7–28.6)
p Value .589 .747 .515
.277
..999 .744 .329 .130 .432 .796
.758 .596
CA 5 cancer antigen. Data are expressed as the mean 6 SD, median (interquartile range [IQR]), or frequency (percentage), as appropriate. a Comorbidities includes diabetes, hypertension, heart disease, and cancer. b Of 12 patients with previous abdominal surgical history in the bipolar coagulation group, 7 underwent Cesarean section, 2 underwent laparoscopic myomectomy, 2 underwent laparoscopic cholecystectomy, and 1 underwent laparoscopic appendectomy. Of 8 patients with previous abdominal surgical history in the suture group, 3 underwent Cesarean section, 2 underwent laparoscopic cholecystectomy, 1 underwent laparoscopic appendectomy, 1 underwent laparotomic appendectomy, and 1 underwent laparotomic myomectomy. c The diameter of the ovarian cyst was measured before surgery via transvaginal and/or transabdominal ultrasound or computed tomography.
the 2 study groups. There were no adverse events, including transfusion, failure of intended surgery, failure of intended ovarian hemostasis (either bipolar coagulation or suture), or intra- or postoperative complications in either group. The ovarian reserve by assessment of AMH levels before and 3 months after surgery are also shown in Table 2. Preoperative AMH levels were also similar between patients in the
2 study groups, at 3.23 ng/mL (IQR, 1.98–4.71) in the bipolar coagulation group and 3.37 ng/mL (IQR, 1.48–5.13) in the suture group (p 5 .941). At 3 months postsurgery, serum AMH levels in the bipolar coagulation and suture groups fell to 1.97 ng/mL (IQR, 0.97–3.43; p , .001) and 2.32 ng/mL (IQR, 0.99–4.32; p , .001), respectively. This meant that the ovarian hemostasis resulted in damage to the ovarian
Table 2 Surgical outcomes Variables
Bipolar coagulation group (n 5 62)
Suture group (n 5 63)
p Value
Adhesiolysis Operative time, min Operative blood loss, mL Change in hemoglobin, mg/dL Length of hospital stay, day (IQR) Ovarian reservea Preoperative AMH level, ng/mL (IQR) Rate of decline in AMH level, % (IQR)
13 (21.0%) 60.3 6 28.0 66.8 6 51.2 1.8 6 0.8 2 (2–3)
15 (23.8%) 59.8 6 24.5 64.3 6 58.5 1.7 6 0.8 2 (2–3)
.703 .898 .448 .331 .292
3.23 (1.98–4.71) 42.2 (16.5–53.0)
3.37 (1.48–5.13) 24.6 (11.6–37.0)
.941 .001
AMH 5 anti-M€ ullerian hormone; IQR 5 interquartile range. Rate of decline was defined as 100 ! (preoperative AMH level 2 postoperative AMH level]/preoperative AMH level. a Ovarian reserve was determined by serial AMH level.
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reserve, regardless of the hemostatic method. Therefore, the rate of decline in serum AMH levels was 42.2% (IQR, 16.5%–53.0%) in the bipolar coagulation group versus 24.6% (IQR, 11.6%–37.0%) in the suture group. The rate of decline in serum AMH levels decreased more in the bipolar coagulation group than in the suture group (p 5 .001). By multivariate analysis, the type of ovarian hemostasis was the only independent variable for the postoperative decrease in ovarian reserve (p 5 .001); the other factors, including the type of ovarian surgery, age, body mass index, and diameter of ovarian cysts had no independent factors. Discussion This study suggests that laparoendoscopic single-site surgery for endometriomas can reduce ovarian reserve, regardless of the ovarian hemostatic method. Our data show that bipolar coagulation after stripping of the endometrioma during LESS-C reduces ovarian reserve more than suturing does, as determined by serial AMH levels. The findings of this study are in agreement with those from other studies [7,12], which concluded that bipolar electrocoagulation following laparoscopic ovarian cystectomy leads to a statistically significant reduction in the basal follicle-stimulating hormone (FSH) levels and antral follicle count (AFC) as parameters of ovarian reserve. Fedele et al compared the postoperative reserve associated with the use of bipolar coagulation (n 5 21) versus ovarian suture (n 5 26) after laparoscopic cystectomy for unilateral endometriomas [12]. At 12-month follow-up, 8 patients (38%) in the bipolar coagulation group had FSH levels .10 mIU/mL versus 3 patients (12%) in the suture group (p 5 .042). They concluded that bipolar coagulation of the ovarian parenchyma after laparoscopic stripping of an endometriotic ovarian cyst adversely affects ovarian function more than suturing does [12]. Coric et al assessed ovarian reserve by AFC following bipolar electrocoagulation versus suturing during laparoscopic ovarian cystectomy [7]. AFC was measured by ultrasound on the third day of 3 postoperative menstrual cycles. The median AFC was significantly higher in sutured ovaries than in electrocoagulated ovaries (p , .05). They concluded that ovarian suturing could be a better hemostatic choice after stripping ovarian endometriomas. However, the results of this study are in contrast to those by Ferrero et al [1]. Ferrero et al assessed ovarian reserve by serial AMH levels pre- and postoperatively in patients who underwent laparoscopic cystectomy for bilateral endometriomas [1]. There was no significant difference in the mean percentage decrease of AMH levels between the 2 study groups after 3 months of follow-up. In our study, all procedures were completed by LESS surgery. We think that the LESS surgery itself does not affect the postoperative change in ovarian reserve. Our opinion is consistent with the result of a randomized controlled trial performed by Yoon et al [13]. They investigated the impact of laparoscopic ovarian cystectomy in various laparoscopic
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settings on ovarian reserve. There was no statistically significant difference in the serial change of AMH levels among the 1-, 2-, and 4-port laparoscopy groups. They concluded that laparoscopic ovarian cystectomy with a reduced port number did not affect the serial change in ovarian reserve. Chang et al performed a prospective longitudinal study to evaluate ovarian reserve changes after laparoscopic cystectomy [14]. Serum AMH levels were serially measured: preoperatively, as well as at 1 week, 1 month, and 3 months after surgery. The median AMH level was 2.23 ng/mL (95% confidence interval [CI], 1.35–3.41 ng/mL) before surgery, but these levels reduced to 0.67 ng/mL (95% CI 0.44–1.70 ng/mL) in the first week after surgery. They then increased to 1.14 ng/mL (95% CI 0.79– 2.36 ng/mL) in the first month and 1.50 ng/mL (95% CI 0.58–3.26 ng/mL) in the third month after surgery [14]. Therefore, this study concluded that ovarian reserve was reduced after laparoscopic cystectomy, but was restored up to 3 months postoperatively in reproductive women [14]. Ferrero et al also investigated changes in ovarian reserve by measuring AMH levels before surgery and at 3, 4, and 12 months after surgery [1]. Patients treated with laparoscopic cystectomy had no significant difference in the percentage change of AMH at 3-, 6-, and 12-month follow-ups after surgery [1]. These observations are in line with the findings of a recent meta-analysis that investigated the effects of surgery for endometriomas on ovarian reserve [15]. Therefore, we measured AMH levels at 3 months after surgery because it was likely that a complete recovery of postoperative ovarian function could be obtained at this point (Table 3). However, further measurement of AMH levels beyond 3 months postsurgery is needed to validate our opinion. Several methods have been proposed for preserving ovarian reserve in patients who require surgical management for ovarian endometriomas: a combination of excision and ablation [17]; the 3-step management technique [10]; the vasopressin injection technique [18]; and the use of hemostatic sealant [9]. Donnez et al proposed a combination of excision and ablation for the treatment of ovarian endometriomas [17]. In a prospective study that included 52 women with unilateral endometriomas, the stripping of the cyst was halted when the ovarian hilus was approached, where the cleavage plane is usually not clearly visible, and a carbon dioxide laser was used to vaporize the remaining 10% to 20% of the endometrioma [17]. The volume of the operated ovaries and the AFC was similar to the nonoperated ovaries 6 months after surgery [17]. A randomized trial on ovarian reserve performed by Tsolakidis et al compared the effects of conventional cystectomy versus 3-step management, which consists of laparoscopic drainage of the endometriotic cyst’s content, administration of a gonadotropin-releasing hormone agonist for 3 months, and a second laparoscopy to vaporize the internal wall of the endometriotic cyst with a carbon dioxide laser [10]. In 20 patients with ovarian
Song et al.
Bipolar Coagulation vs Suture in Preserving Ovarian Reserve
419
Table 3 Postoperative ovarian reserves according to various hemostatic methods No. of patients
Pathologic finding
Laterality
Endometrioma (n 5 13) Nonendometrioma (n 5 7) Endometrioma (n 5 45)
Unilateral (n 5 13) Bilateral (n 5 7) Unilateral (n 5 45)
Endometrioma (n 5 100)
Bilateral (n 5 100)
59
Non-endometrioma (n 5 59)
Unilateral (n 5 59)
30.3 6 5.0
87
Endometrioma (n 5 50) Non-endometrioma (n 5 37)
Unilateral (n 5 59) Bilateral (n 5 28)
RCT
31.2 6 5.9
100
Prospective cohort
31.0 6 4.9
125
Endometrioma (n 5 56) Non-endometrioma (n 5 44) Endometrioma (n 5 125)
Unilateral (n 5 79) Bilateral (n 5 21) Unilateral (n 5 94) Bilateral (n 5 31)
Author
Design
Age (yr)
Chang [14]
Prospective cohort
33.8 6 7.2
20
Coric [7]
RCT
30.3 (21–35)
45
Ferrero [1]
RCT
32.0 6 3.9
100
Mohamed [16]
RCT
23.5 6 4.6
Yoon [13]
RCT
Song [9]
Present study
Intervention (ovarian hemostasis)
Follow-up (mos)
Outcome measurement
Bipolar coagulation (n 5 20)
3
AMH, ovarian volume
Bipolar coagulation (n 5 22) Ovarian suture (n 5 23) Bipolar coagulation (n 5 22) Ovarian suture (n 5 23) Laparoscopy (n 5 30) Laparotomy (n 5 29) SPA laparoscopy (n 5 29) TPA laparoscopy (n 5 29) FPA laparoscopy (n 5 29) Bipolar coagulation (n 5 50) Hemostatic sealant (n 5 50) Bipolar coagulation (n 5 62) Ovarian suture (n 5 63)
3
AFCa
12
AMH, FSHb
6
AMH, AFC, PSVc
3
AMHd
3
AMHe
3
AMH
AFC 5 antral follicle count; FPA 5 4-port access; PSV 5 ovarian stromal peak systolic velocity; RCT 5 randomized control trial; SPA 5 single-port access; TPA, 2-port access. a The median AFC was significantly higher in the suture group than in the bipolar coagulation group (12 [9–19] vs 5.0 [2–10], p , .05). b The mean percentage increase in basal FSH was higher in the bipolar coagulation group than in the suture group at both 3- (p 5 .023) and 6-month follow-up (p 5 .029), but not at 12-month follow-up. There was no significant difference in the mean percentage decrease of AMH levels in the bipolar coagulation group and the suture group at 3-, 6-, and 12-month follow-up. c Laparoscopic ovarian cystectomy is associated with a significant reduction in ovarian reserve. d There was no statistically significant difference in the serial change of AMH levels among the 1-, 2, and 4-port laparoscopy groups. e The rate of decline of AMH levels was significantly greater in the bipolar coagulation group than the hemostatic sealant group (41.2% [interquartile range, 17.2%–54.5%] and 16.1% [interquartile range, 8.3%–44.7%], respectively; p 5 .004).
endometriomas, patients who underwent the 3-step management technique had better ovarian reserve as assessed by serial AMH levels than those underwent conventional 1-step cystectomy [10]. The vasopressin injection technique has been also proposed to preserve ovarian reserve during the stripping of endometriotic cysts [18]. A randomized controlled trial that included 15 women with a unilateral endometrioma suggested that the injection of vasopressin during laparoscopic excision of endometriomas reduced the use of coagulation, thereby protecting ovarian reserve [18]. Song et al also proposed the use of hemostatic sealant (FloSeal; Baxter Healthcare Corporation,
Deerfield, Illinois) to control postcystectomy ovarian wound ground bleeding [9]. A randomized controlled trial of 100 women with benign ovarian cysts showed that hemostatic sealant diminished postoperative ovarian reserve, as determined by serial AMH levels, less than bipolar coagulation did [9]. This study had some limitations. First, this study had a nonrandomized comparative design, although quasirandomization was used to allocate patients to a treatment. We had no ability and facility to manage the randomization process. This might have weakened our results. Second, we did not assess other markers of ovarian reserve, such as
420
sonographic markers (AFC, ovarian volume, and peak systolic velocity of the ovarian stromal vasculature) or serum markers (basal FSH and inhibin-B), although the level of serum AMH was recently accepted as the most reliable and easily measurable marker for postoperative assessment of ovarian reserve [19–22]. Third, we did not use new second-generation bipolar electrosurgical devices, such as LigaSure (Valleylab, Boulder, CO), EnSeal (Ethicon, Cincinnati, OH), or Thunderbeat (Olympus, Tokyo, Japan). Therefore, our results might not be applicable to other device settings. In conclusion, sutures diminished postoperative ovarian reserve, as determined by pre- and 3-month postoperative AMH levels, less than bipolar coagulation did. Therefore, suturing may be a better choice as a method of hemostasis after stripping ovarian endometriomas. However, further randomized controlled trials are needed to confirm the findings of this study. References 1. Ferrero S, Venturini PL, Gillott DJ, Remorgida V. Leone Roberti Maggiore U. Hemostasis by bipolar coagulation versus suture after surgical stripping of bilateral ovarian endometriomas: a randomized controlled trial. J Minim Invasive Gynecol. 2012;19:722–730. 2. Celik HG, Dogan E, Okyay E, et al. Effect of laparoscopic excision of endometriomas on ovarian reserve: serial changes in the serum antimullerian hormone levels. Fertil Steril. 2012;97:1472–1478. 3. Vercellini P, Fedele L, Aimi G, De Giorgi O, Consonni D, Crosignani PG. Reproductive performance, pain recurrence and disease relapse after conservative surgical treatment for endometriosis: the predictive value of the current classification system. Hum Reprod. 2006;21: 2679–2685. 4. Broekmans FJ, Kwee J, Hendriks DJ, Mol BW, Lambalk CB. A systematic review of tests predicting ovarian reserve and IVF outcome. Hum Reprod Update. 2006;12:685–718. 5. Ditto A, Martinelli F, Lorusso D, Haeusler E, Carcangiu M, Raspagliesi F. Fertility sparing surgery in early stage epithelial ovarian cancer. J Gynecol Oncol. 2014;25:320–327. 6. Choi WK, Kim JK, Yang JB, Ko YB, Nam SL, Lee KH. Two-port access versus four-port access laparoscopic ovarian cystectomy. Obstet Gynecol Sci. 2014;57:379–385. 7. Coric M, Barisic D, Pavicic D, Karadza M, Banovic M. Electrocoagulation versus suture after laparoscopic stripping of ovarian endometriomas assessed by antral follicle count: preliminary results of randomized clinical trial. Arch Gynecol Obstet. 2011;283:373–378. 8. Hirokawa W, Iwase A, Goto M, et al. The post-operative decline in serum anti-Mullerian hormone correlates with the bilaterality and severity of endometriosis. Hum Reprod. 2011;26:904–910.
Journal of Minimally Invasive Gynecology, Vol 22, No 3, March/April 2015 9. Song T, Lee SH, Kim WY. Additional benefit of hemostatic sealant in preservation of ovarian reserve during laparoscopic ovarian cystectomy: a multi-center, randomized controlled trial. Hum Reprod. 2014;29:1659–1665. 10. Tsolakidis D, Pados G, Vavilis D, et al. The impact on ovarian reserve after laparoscopic ovarian cystectomy versus three-stage management in patients with endometriomas: a prospective randomized study. Fertil Steril. 2010;94:71–77. 11. Var T, Batioglu S, Tonguc E, Kahyaoglu I. The effect of laparoscopic ovarian cystectomy versus coagulation in bilateral endometriomas on ovarian reserve as determined by antral follicle count and ovarian volume: a prospective randomized study. Fertil Steril. 2011;95: 2247–2250. 12. Fedele L, Bianchi S, Zanconato G, Bergamini V, Berlanda N. Bipolar electrocoagulation versus suture of solitary ovary after laparoscopic excision of ovarian endometriomas. J Am Assoc Gynecol Laparosc. 2004;11:344–347. 13. Yoon BS, Kim YS, Seong SJ, et al. Impact on ovarian reserve after laparoscopic ovarian cystectomy with reduced port number: a randomized controlled trial. Eur J Obstet Gynecol Reprod Biol. 2014;176: 34–38. 14. Chang HJ, Han SH, Lee JR, et al. Impact of laparoscopic cystectomy on ovarian reserve: serial changes of serum anti-Mullerian hormone levels. Fertil Steril. 2010;94:343–349. 15. Raffi F, Metwally M, Amer S. The impact of excision of ovarian endometrioma on ovarian reserve: a systematic review and meta-analysis. J Clin Endocrinol Metab. 2012;97:3146–3154. 16. Mohamed ML, Nouh AA, El-Behery MM, Mansour SA. Effect on ovarian reserve of laparoscopic bipolar electrocoagulation versus laparotomic hemostatic sutures during unilateral ovarian cystectomy. Int J Gynaecol Obstet. 2011;114:69–72. 17. Donnez J, Lousse JC, Jadoul P, Donnez O, Squifflet J. Laparoscopic management of endometriomas using a combined technique of excisional (cystectomy) and ablative surgery. Fertil Steril. 2010;94:28–32. 18. Saeki A, Matsumoto T, Ikuma K, et al. The vasopressin injection technique for laparoscopic excision of ovarian endometrioma: a technique to reduce the use of coagulation. J Minim Invasive Gynecol. 2010;17: 176–179. 19. Fanchin R, Schonauer LM, Righini C, Guibourdenche J, Frydman R, Taieb J. Serum anti-Mullerian hormone is more strongly related to ovarian follicular status than serum inhibin B, estradiol, FSH and LH on day 3. Hum Reprod. 2003;18:323–327. 20. Kwee J, Schats R, McDonnell J, Themmen A, de Jong F, Lambalk C. Evaluation of anti-Mullerian hormone as a test for the prediction of ovarian reserve. Fertil Steril. 2008;90:737–743. 21. McIlveen M, Skull JD, Ledger WL. Evaluation of the utility of multiple endocrine and ultrasound measures of ovarian reserve in the prediction of cycle cancellation in a high-risk IVF population. Hum Reprod. 2007; 22:778–785. 22. Seifer DB, MacLaughlin DT, Christian BP, Feng B, Shelden RM. Early follicular serum mullerian-inhibiting substance levels are associated with ovarian response during assisted reproductive technology cycles. Fertil Steril. 2002;77:468–471.
Effect on Ovarian Reserve of Hemostasis by Bipolar Coagulation Versus Suture During Laparoendoscopic Single-Site Cystectomy for Ovarian Endometriomas Taejong Song, MD, PhD*, Woo Young Kim, MD, Kyo Won Lee, MD, PhD, and Kye Hyun Kim, MD, PhD From the Department of Obstetrics & Gynecology, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea (Drs. Song, W. Y. Kim, Lee, and K. H. Kim), and Department of Obstetrics & Gynecology, CHA Gangnam Medical Center, CHA University, Seoul, Republic of Korea (Dr. Song).
ABSTRACT Study Objective: To compare the postoperative decrease in ovarian reserve between hemostasis by bipolar coagulation and suture during laparoendoscopic single-site cystectomy (LESS-C) for ovarian endometriomas. Design: Prospective comparative study (Canadian Task Force Classification II-1). Setting: University hospital. Patients: One hundred twenty-five patients with ovarian endometriomas. Interventions: Patients with endometrioma were managed by hemostasis with either bipolar coagulation (n 5 62) or suturing (n 5 63) during LESS-C. We evaluated the impact of surgery on ovarian reserve using serum anti-M€ ullerian hormone (AMH) levels, which were measured before surgery and 3 months after surgery in all patients. Measurement and Main Results: Baseline characteristics such as age, bilaterality of endometriomas, and preoperative AMH levels were similar between the 2 study groups. There were also no differences between the 2 groups in surgical outcomes, such as operative time, operative blood loss, or operative complications. In both study groups, postoperative AMH levels were lower than preoperative AMH levels (p , .001). The decline rate of AMH levels was significantly greater in the bipolar coagulation group than in the suture group (42.2% [interquartile range, 16.5%–53.0%] and 24.6% [interquartile range, 11.6%– 37.0%], respectively, p 5 .001). Conclusion: Hemostasis by bipolar coagulation after stripping of the endometrioma during LESS-C reduces ovarian reserve more than suturing does, as determined by serial AMH levels. Therefore, suturing may be a better hemostatic choice after stripping ovarian endometriomas. Journal of Minimally Invasive Gynecology (2015) 22, 415–420 Ó 2015 AAGL. All rights reserved. Keywords:
AMH; Bipolar coagulation; Ovarian cystectomy; Ovarian reserve; Suture
DISCUSS
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Laparoscopic cystectomy is a well-established method of management for ovarian endometriomas [1–6]. The surgical procedure is usually performed by stripping the Corresponding author: Taejong Song, MD, PhD, Department of Obstetrics & Gynecology, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, 108 Pyung-dong, Jongno-gu, Seoul 110-746, Republic of Korea. E-mail: [email protected] Submitted September 3, 2014. Accepted for publication November 6, 2014. Available at www.sciencedirect.com and www.jmig.org 1553-4650/$ - see front matter Ó 2015 AAGL. All rights reserved. http://dx.doi.org/10.1016/j.jmig.2014.11.002
endometriotic cyst wall, followed by bleeding control of the ovarian wound ground using bipolar coagulation or suturing. However, the ovarian hemostasis achieved by these 2 methods could result in damage to the ovarian reserve [7–11]. Bipolar coagulation can result in thermal destruction of the surrounding healthy ovarian follicle, whereas a hemostatic suture may result in mechanical damage to normal ovarian tissue and an increase in intraovarian pressure in ischemic regions. Studies that have compared hemostasis by bipolar coagulation versus suturing during laparoscopic ovarian
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cystectomy have not shown consistent effects on ovarian reserve [1,7,12]. Furthermore, no study that has compared these 2 hemostatic methods has been performed in the setting of laparoendoscopic single-site ovarian cystectomy (LESS-C). Because of the increasing patient demand for LESS-C, it is important to determine which hemostatic methods better preserve postoperative ovarian reserve. Therefore, we compared the effects of bipolar coagulation versus suturing on ovarian reserve in patients who underwent LESS-C for ovarian endometriomas. Materials and Methods This was a prospective nonrandomized study of 125 patients who underwent LESS-C for endometriomas between October 2011 and May 2014 at the CHA Gangnam Medical Center, Seoul, Republic of Korea. The 62 patients who underwent LESS-C with hemostasis by bipolar coagulation were compared with 63 patients who underwent LESS-C with hemostasis by suturing to control bleeding from the ovarian wound ground. Group allocation was carried out according to an odd or even procedure, with the first patient being allocated to the suture group, the second to the bipolar coagulation group, and so on. Patients between 18 and 39 years of age, with a maximum diameter of the endometriotic cyst between 3 and 12 cm, regular menstrual bleeding (defined as cycle length between 21 and 45 days), and appropriate medical status for laparoscopic surgery (American Society of Anesthesiologists Physical Status classification 1 or 2) were included in this study. Patients with any suspicious findings of malignant gynecologic disease, postmenopausal status, pregnancy, lactation, any other endocrine disease (such as uncontrolled thyroid dysfunction, hyperprolactinemia, or Cushing syndrome), or use of hormonal treatments in the 3 months before surgery were excluded. After obtaining institutional review board approval for this study, all patients gave written consent for their data to be collected prospectively. All procedures were performed by 1 surgeon (T. Song), who previously managed .200 LESS-C procedures. All patients underwent the same standard preparation before surgery, including the administration of prophylactic antibiotics 30 min before the procedure. The LESS-C technique used was previously described in detail [9]. In brief, after the introduction of general anesthesia, a single multichannel port was inserted through the umbilicus, and a laparoscope was introduced through 1 of the channels. Before initiating the stripping of the endometriotic cyst, the ovary was completely freed by obtuse and sharp dissection. After identifying a cleavage plane between the cyst wall and the ovarian cortex, the ovary was pulled slowly and gently in opposite directions with 2 atraumatic grasping forceps. Once the whole cystic wall was separated from the ovarian cortex, bipolar coagulation or ovarian suturing was applied for hemostasis. In the bipolar coagulation group, complete hemostasis was achieved with a 20- to 30-W current applied using bipolar forceps (Karl Storz, Tuttlingen, Germany) on sites of bleeding in the internal face of the ovary without coagulation of external surface. Bleeding sites were then re-examined by irrigation. In the suture group, hemostasis of the ovarian parenchyma was achieved using a 12-in, 2-0 unidirectional-barbed suture with a 26-mm half circle taper-point needle (V-Loc 90 Absorbable Wound Closure device; Covidien, Mansfield, Massachusetts). The first stitch was locked
Journal of Minimally Invasive Gynecology, Vol 22, No 3, March/April 2015
by a loop at 1 end of the ovarian wound, and then a continuous suture was passed through to the opposite end of the ovarian wound and cut without tying a knot. The ovary was sutured edge-to-edge. No chemical hemostats, except for bipolar coagulation or ovarian suture were allowed in either group. In the bipolar group, no bipolar coagulation was performed during or after stripping of the cysts. The ovarian cysts, which were placed into the specimen retrieval endopouch, were removed through the umbilical single-port. After bleeding was controlled, the single multichannel port was removed, the transumbilical fascia and subcutaneous tissue were approximated and closed layer by layer with 1-0 Vicryl (Ethicon, Somerville, New Jersey), and the skin was closed subcuticularly with 3-0 Vicryl. The primary aim of this study was to compare the effects of 2 hemostatic techniques (bipolar coagulation vs suturing) on ovarian reserve in patients who underwent LESS-C for ovarian endometriomas. The ovarian reserve was assessed by measuring serum AMH levels, which were measured before surgery and 3 months after surgery in all patients. The rate of decline of serum AMH levels was defined as follows: rate of decline (%) 5 100 ! (preoperative AMH level – postoperative AMH level)/preoperative AMH level. The serum was separated from whole blood, transferred to polypropylene tubes, and stored at –70 C until the assay. Serum AMH concentrations were determined using a commercially available enzyme-linked immunosorbent assay kit (Beckman Coulter, Marseille, France). The detection limit of the assay was 0.14 ng/mL, and the intra- and inter-assay coefficients of variation for the AMH assay were .12.3% and .14.2%, respectively. All statistical analyses were performed using SPSS 13.0 (SPSS Inc., Chicago, Illinois). Data are presented as means 6 SD or medians (interquartile range [IQR]) for continuous variables, and frequencies (percentages) for categorical variables. Baseline parameters and study outcomes were compared between the 2 groups using the Student’s t-test or the Mann-Whitney test for continuous variables, and the c2 test or Fisher’s exact test for categorical variables, as appropriate. The serum AMH levels before and after surgery were compared in the same group using the Wilcoxon signed-rank test. Multivariate analysis to determine independent parameters for postoperative ovarian reserve was performed using multiple linear regression. p Values ,.05 were considered statistically significant.
Results Baseline characteristics including age, body mass index, parity, marital status, and abdominal surgical history were similar between the 2 study groups (Table 1). The diameter and location of ovarian cysts and the level of preoperative tumor markers (e.g., cancer antigen-125 and cancer antigen 19-9) also did not differ between the 2 groups. The surgical outcomes of each group are shown in Table 2. The histologic type of ovarian cyst, ovarian surgery performed, operative time (defined as the time from skin incision to skin closure), operative blood loss (calculated as the difference between suction and irrigation), change in hemoglobin (defined as the difference between preoperative hemoglobin level and that at postoperative day 1), and length of hospital stay (defined as the time from the operation day to the day of discharge) were all similar between
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Table 1 Baseline characteristics Characteristics
Bipolar coagulation group (n 5 62)
Suture group (n 5 63)
Age, yrs Body mass index, kg/m2 Marital status Married or cohabitating Single/separated/widowed/Divorced Parity Nulliparous Parous Menopause Comorbiditiesa Abdominal surgical historyb Preoperative hemoglobin (mg/dL) Diameter of ovarian cyst, cmc Location of ovarian cyst Unilateral Bilateral CA125, IU/mL (IQR) CA19-9, IU/mL (IQR)
31.2 6 4.8 20.6 6 2.6
30.8 6 5.2 20.4 6 2.6
38 (61.3%) 24 (38.7%)
35 (55.6%) 28 (44.4%)
46 (74.2%) 16 (25.8%) 0 4 (6.5%) 12 (19.4%) 12.7 6 0.9 6.4 6 1.6
51 (82.3%) 11 (17.7%) 0 6 (9.5%) 8 (12.9%) 12.9 6 1.0 6.8 6 2.2
46 (74.2%) 16 (25.8%) 25.8 (15.0–48.8) 20.6 (9.4–36.2)
48 (76.2%) 15 (23.8%) 22.2 (14.0–42.9) 17.1 (11.7–28.6)
p Value .589 .747 .515
.277
..999 .744 .329 .130 .432 .796
.758 .596
CA 5 cancer antigen. Data are expressed as the mean 6 SD, median (interquartile range [IQR]), or frequency (percentage), as appropriate. a Comorbidities includes diabetes, hypertension, heart disease, and cancer. b Of 12 patients with previous abdominal surgical history in the bipolar coagulation group, 7 underwent Cesarean section, 2 underwent laparoscopic myomectomy, 2 underwent laparoscopic cholecystectomy, and 1 underwent laparoscopic appendectomy. Of 8 patients with previous abdominal surgical history in the suture group, 3 underwent Cesarean section, 2 underwent laparoscopic cholecystectomy, 1 underwent laparoscopic appendectomy, 1 underwent laparotomic appendectomy, and 1 underwent laparotomic myomectomy. c The diameter of the ovarian cyst was measured before surgery via transvaginal and/or transabdominal ultrasound or computed tomography.
the 2 study groups. There were no adverse events, including transfusion, failure of intended surgery, failure of intended ovarian hemostasis (either bipolar coagulation or suture), or intra- or postoperative complications in either group. The ovarian reserve by assessment of AMH levels before and 3 months after surgery are also shown in Table 2. Preoperative AMH levels were also similar between patients in the
2 study groups, at 3.23 ng/mL (IQR, 1.98–4.71) in the bipolar coagulation group and 3.37 ng/mL (IQR, 1.48–5.13) in the suture group (p 5 .941). At 3 months postsurgery, serum AMH levels in the bipolar coagulation and suture groups fell to 1.97 ng/mL (IQR, 0.97–3.43; p , .001) and 2.32 ng/mL (IQR, 0.99–4.32; p , .001), respectively. This meant that the ovarian hemostasis resulted in damage to the ovarian
Table 2 Surgical outcomes Variables
Bipolar coagulation group (n 5 62)
Suture group (n 5 63)
p Value
Adhesiolysis Operative time, min Operative blood loss, mL Change in hemoglobin, mg/dL Length of hospital stay, day (IQR) Ovarian reservea Preoperative AMH level, ng/mL (IQR) Rate of decline in AMH level, % (IQR)
13 (21.0%) 60.3 6 28.0 66.8 6 51.2 1.8 6 0.8 2 (2–3)
15 (23.8%) 59.8 6 24.5 64.3 6 58.5 1.7 6 0.8 2 (2–3)
.703 .898 .448 .331 .292
3.23 (1.98–4.71) 42.2 (16.5–53.0)
3.37 (1.48–5.13) 24.6 (11.6–37.0)
.941 .001
AMH 5 anti-M€ ullerian hormone; IQR 5 interquartile range. Rate of decline was defined as 100 ! (preoperative AMH level 2 postoperative AMH level]/preoperative AMH level. a Ovarian reserve was determined by serial AMH level.
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reserve, regardless of the hemostatic method. Therefore, the rate of decline in serum AMH levels was 42.2% (IQR, 16.5%–53.0%) in the bipolar coagulation group versus 24.6% (IQR, 11.6%–37.0%) in the suture group. The rate of decline in serum AMH levels decreased more in the bipolar coagulation group than in the suture group (p 5 .001). By multivariate analysis, the type of ovarian hemostasis was the only independent variable for the postoperative decrease in ovarian reserve (p 5 .001); the other factors, including the type of ovarian surgery, age, body mass index, and diameter of ovarian cysts had no independent factors. Discussion This study suggests that laparoendoscopic single-site surgery for endometriomas can reduce ovarian reserve, regardless of the ovarian hemostatic method. Our data show that bipolar coagulation after stripping of the endometrioma during LESS-C reduces ovarian reserve more than suturing does, as determined by serial AMH levels. The findings of this study are in agreement with those from other studies [7,12], which concluded that bipolar electrocoagulation following laparoscopic ovarian cystectomy leads to a statistically significant reduction in the basal follicle-stimulating hormone (FSH) levels and antral follicle count (AFC) as parameters of ovarian reserve. Fedele et al compared the postoperative reserve associated with the use of bipolar coagulation (n 5 21) versus ovarian suture (n 5 26) after laparoscopic cystectomy for unilateral endometriomas [12]. At 12-month follow-up, 8 patients (38%) in the bipolar coagulation group had FSH levels .10 mIU/mL versus 3 patients (12%) in the suture group (p 5 .042). They concluded that bipolar coagulation of the ovarian parenchyma after laparoscopic stripping of an endometriotic ovarian cyst adversely affects ovarian function more than suturing does [12]. Coric et al assessed ovarian reserve by AFC following bipolar electrocoagulation versus suturing during laparoscopic ovarian cystectomy [7]. AFC was measured by ultrasound on the third day of 3 postoperative menstrual cycles. The median AFC was significantly higher in sutured ovaries than in electrocoagulated ovaries (p , .05). They concluded that ovarian suturing could be a better hemostatic choice after stripping ovarian endometriomas. However, the results of this study are in contrast to those by Ferrero et al [1]. Ferrero et al assessed ovarian reserve by serial AMH levels pre- and postoperatively in patients who underwent laparoscopic cystectomy for bilateral endometriomas [1]. There was no significant difference in the mean percentage decrease of AMH levels between the 2 study groups after 3 months of follow-up. In our study, all procedures were completed by LESS surgery. We think that the LESS surgery itself does not affect the postoperative change in ovarian reserve. Our opinion is consistent with the result of a randomized controlled trial performed by Yoon et al [13]. They investigated the impact of laparoscopic ovarian cystectomy in various laparoscopic
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settings on ovarian reserve. There was no statistically significant difference in the serial change of AMH levels among the 1-, 2-, and 4-port laparoscopy groups. They concluded that laparoscopic ovarian cystectomy with a reduced port number did not affect the serial change in ovarian reserve. Chang et al performed a prospective longitudinal study to evaluate ovarian reserve changes after laparoscopic cystectomy [14]. Serum AMH levels were serially measured: preoperatively, as well as at 1 week, 1 month, and 3 months after surgery. The median AMH level was 2.23 ng/mL (95% confidence interval [CI], 1.35–3.41 ng/mL) before surgery, but these levels reduced to 0.67 ng/mL (95% CI 0.44–1.70 ng/mL) in the first week after surgery. They then increased to 1.14 ng/mL (95% CI 0.79– 2.36 ng/mL) in the first month and 1.50 ng/mL (95% CI 0.58–3.26 ng/mL) in the third month after surgery [14]. Therefore, this study concluded that ovarian reserve was reduced after laparoscopic cystectomy, but was restored up to 3 months postoperatively in reproductive women [14]. Ferrero et al also investigated changes in ovarian reserve by measuring AMH levels before surgery and at 3, 4, and 12 months after surgery [1]. Patients treated with laparoscopic cystectomy had no significant difference in the percentage change of AMH at 3-, 6-, and 12-month follow-ups after surgery [1]. These observations are in line with the findings of a recent meta-analysis that investigated the effects of surgery for endometriomas on ovarian reserve [15]. Therefore, we measured AMH levels at 3 months after surgery because it was likely that a complete recovery of postoperative ovarian function could be obtained at this point (Table 3). However, further measurement of AMH levels beyond 3 months postsurgery is needed to validate our opinion. Several methods have been proposed for preserving ovarian reserve in patients who require surgical management for ovarian endometriomas: a combination of excision and ablation [17]; the 3-step management technique [10]; the vasopressin injection technique [18]; and the use of hemostatic sealant [9]. Donnez et al proposed a combination of excision and ablation for the treatment of ovarian endometriomas [17]. In a prospective study that included 52 women with unilateral endometriomas, the stripping of the cyst was halted when the ovarian hilus was approached, where the cleavage plane is usually not clearly visible, and a carbon dioxide laser was used to vaporize the remaining 10% to 20% of the endometrioma [17]. The volume of the operated ovaries and the AFC was similar to the nonoperated ovaries 6 months after surgery [17]. A randomized trial on ovarian reserve performed by Tsolakidis et al compared the effects of conventional cystectomy versus 3-step management, which consists of laparoscopic drainage of the endometriotic cyst’s content, administration of a gonadotropin-releasing hormone agonist for 3 months, and a second laparoscopy to vaporize the internal wall of the endometriotic cyst with a carbon dioxide laser [10]. In 20 patients with ovarian
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Table 3 Postoperative ovarian reserves according to various hemostatic methods No. of patients
Pathologic finding
Laterality
Endometrioma (n 5 13) Nonendometrioma (n 5 7) Endometrioma (n 5 45)
Unilateral (n 5 13) Bilateral (n 5 7) Unilateral (n 5 45)
Endometrioma (n 5 100)
Bilateral (n 5 100)
59
Non-endometrioma (n 5 59)
Unilateral (n 5 59)
30.3 6 5.0
87
Endometrioma (n 5 50) Non-endometrioma (n 5 37)
Unilateral (n 5 59) Bilateral (n 5 28)
RCT
31.2 6 5.9
100
Prospective cohort
31.0 6 4.9
125
Endometrioma (n 5 56) Non-endometrioma (n 5 44) Endometrioma (n 5 125)
Unilateral (n 5 79) Bilateral (n 5 21) Unilateral (n 5 94) Bilateral (n 5 31)
Author
Design
Age (yr)
Chang [14]
Prospective cohort
33.8 6 7.2
20
Coric [7]
RCT
30.3 (21–35)
45
Ferrero [1]
RCT
32.0 6 3.9
100
Mohamed [16]
RCT
23.5 6 4.6
Yoon [13]
RCT
Song [9]
Present study
Intervention (ovarian hemostasis)
Follow-up (mos)
Outcome measurement
Bipolar coagulation (n 5 20)
3
AMH, ovarian volume
Bipolar coagulation (n 5 22) Ovarian suture (n 5 23) Bipolar coagulation (n 5 22) Ovarian suture (n 5 23) Laparoscopy (n 5 30) Laparotomy (n 5 29) SPA laparoscopy (n 5 29) TPA laparoscopy (n 5 29) FPA laparoscopy (n 5 29) Bipolar coagulation (n 5 50) Hemostatic sealant (n 5 50) Bipolar coagulation (n 5 62) Ovarian suture (n 5 63)
3
AFCa
12
AMH, FSHb
6
AMH, AFC, PSVc
3
AMHd
3
AMHe
3
AMH
AFC 5 antral follicle count; FPA 5 4-port access; PSV 5 ovarian stromal peak systolic velocity; RCT 5 randomized control trial; SPA 5 single-port access; TPA, 2-port access. a The median AFC was significantly higher in the suture group than in the bipolar coagulation group (12 [9–19] vs 5.0 [2–10], p , .05). b The mean percentage increase in basal FSH was higher in the bipolar coagulation group than in the suture group at both 3- (p 5 .023) and 6-month follow-up (p 5 .029), but not at 12-month follow-up. There was no significant difference in the mean percentage decrease of AMH levels in the bipolar coagulation group and the suture group at 3-, 6-, and 12-month follow-up. c Laparoscopic ovarian cystectomy is associated with a significant reduction in ovarian reserve. d There was no statistically significant difference in the serial change of AMH levels among the 1-, 2, and 4-port laparoscopy groups. e The rate of decline of AMH levels was significantly greater in the bipolar coagulation group than the hemostatic sealant group (41.2% [interquartile range, 17.2%–54.5%] and 16.1% [interquartile range, 8.3%–44.7%], respectively; p 5 .004).
endometriomas, patients who underwent the 3-step management technique had better ovarian reserve as assessed by serial AMH levels than those underwent conventional 1-step cystectomy [10]. The vasopressin injection technique has been also proposed to preserve ovarian reserve during the stripping of endometriotic cysts [18]. A randomized controlled trial that included 15 women with a unilateral endometrioma suggested that the injection of vasopressin during laparoscopic excision of endometriomas reduced the use of coagulation, thereby protecting ovarian reserve [18]. Song et al also proposed the use of hemostatic sealant (FloSeal; Baxter Healthcare Corporation,
Deerfield, Illinois) to control postcystectomy ovarian wound ground bleeding [9]. A randomized controlled trial of 100 women with benign ovarian cysts showed that hemostatic sealant diminished postoperative ovarian reserve, as determined by serial AMH levels, less than bipolar coagulation did [9]. This study had some limitations. First, this study had a nonrandomized comparative design, although quasirandomization was used to allocate patients to a treatment. We had no ability and facility to manage the randomization process. This might have weakened our results. Second, we did not assess other markers of ovarian reserve, such as
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sonographic markers (AFC, ovarian volume, and peak systolic velocity of the ovarian stromal vasculature) or serum markers (basal FSH and inhibin-B), although the level of serum AMH was recently accepted as the most reliable and easily measurable marker for postoperative assessment of ovarian reserve [19–22]. Third, we did not use new second-generation bipolar electrosurgical devices, such as LigaSure (Valleylab, Boulder, CO), EnSeal (Ethicon, Cincinnati, OH), or Thunderbeat (Olympus, Tokyo, Japan). Therefore, our results might not be applicable to other device settings. In conclusion, sutures diminished postoperative ovarian reserve, as determined by pre- and 3-month postoperative AMH levels, less than bipolar coagulation did. Therefore, suturing may be a better choice as a method of hemostasis after stripping ovarian endometriomas. However, further randomized controlled trials are needed to confirm the findings of this study. References 1. Ferrero S, Venturini PL, Gillott DJ, Remorgida V. Leone Roberti Maggiore U. Hemostasis by bipolar coagulation versus suture after surgical stripping of bilateral ovarian endometriomas: a randomized controlled trial. J Minim Invasive Gynecol. 2012;19:722–730. 2. Celik HG, Dogan E, Okyay E, et al. Effect of laparoscopic excision of endometriomas on ovarian reserve: serial changes in the serum antimullerian hormone levels. Fertil Steril. 2012;97:1472–1478. 3. Vercellini P, Fedele L, Aimi G, De Giorgi O, Consonni D, Crosignani PG. Reproductive performance, pain recurrence and disease relapse after conservative surgical treatment for endometriosis: the predictive value of the current classification system. Hum Reprod. 2006;21: 2679–2685. 4. Broekmans FJ, Kwee J, Hendriks DJ, Mol BW, Lambalk CB. A systematic review of tests predicting ovarian reserve and IVF outcome. Hum Reprod Update. 2006;12:685–718. 5. Ditto A, Martinelli F, Lorusso D, Haeusler E, Carcangiu M, Raspagliesi F. Fertility sparing surgery in early stage epithelial ovarian cancer. J Gynecol Oncol. 2014;25:320–327. 6. Choi WK, Kim JK, Yang JB, Ko YB, Nam SL, Lee KH. Two-port access versus four-port access laparoscopic ovarian cystectomy. Obstet Gynecol Sci. 2014;57:379–385. 7. Coric M, Barisic D, Pavicic D, Karadza M, Banovic M. Electrocoagulation versus suture after laparoscopic stripping of ovarian endometriomas assessed by antral follicle count: preliminary results of randomized clinical trial. Arch Gynecol Obstet. 2011;283:373–378. 8. Hirokawa W, Iwase A, Goto M, et al. The post-operative decline in serum anti-Mullerian hormone correlates with the bilaterality and severity of endometriosis. Hum Reprod. 2011;26:904–910.
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